Situation of Pediatric Patients with Testicular Torsion in Times of COVID-19

Purpose. To assess whether the COVID-19 pandemic had an influence on presentation of testicular torsion and/or increase in the frequency of orchiectomy. Patients and Methods. This retrospective study included boys under 18 years of age with testicular torsion divided in two groups: pre-COVID operated in 2019 vs. COVID-19 group from 2020. We compared demographic data as well as local and general symptoms. We analyzed additional tests, intraoperative findings, length of operation and hospitalization, and followup. Results. We analyzed the data collected from 44 patients (24 boys from first group vs. 20 boys from second group). The median age was 13.4 years vs. 14.5 years in the latter. The median time of symptoms duration was 6.5 hours and 8.5 hours, respectively. The main manifestation was testicular pain without additional signs. The results of the laboratory tests did not reflect local advancement. In the 2019 group, Doppler ultrasound showed absent blood flow in the affected testicle in 62% vs. 80% in 2020. The mean time from admission to surgery was virtually identical: 75 minutes in 2019 vs. 76 minutes in 2020. The mean duration of scrotal revision was similar in both groups. There was only one significant difference: the degree of twisting. In 2019, the mean was 360° vs. 540° in 2020. Incidence of orchiectomy also did not significantly vary between the analyzed time periods, with 21% during the pandemic and 35% during the pre-COVID-19 period. Conclusion. We did not observe an increase in the number of testicular torsion cases during the COVID-19 pandemic. Most importantly, the rates of orchiectomy did not significantly differ between the patients with testicular torsion presenting during the COVID-19 outbreak.


Introduction
Acute scrotal pain, with or without scrotal swelling and skin redness, is one of the manifestations of acute scrotum and always requires prompt diagnosis [1]. Tere are three main causes of acute scrotum in children: testicular torsion, testicular appendage torsion, and epididymo-orchitis [2]. Testicular torsion is one of the most common pediatric emergencies, and it should always be excluded in all patients with acute scrotum. Testicle survival after a torsion event depends primarily on the time of surgical intervention. Early surgery within 6 hours from the onset of symptoms results in a testicular salvage rate of up to 90-97% [3].
In our survey, we wanted to analyze how COVID-19 pandemic lockdown measures infuenced the incidence of orchiectomy in boys with testicular torsion. Te World Health Organization (WHO) declared the COVID-19 pandemic in March 2020 [4]. In Poland, the frst ofcial case of COVID-19 was also reported in March 2020. Despite pandemic restrictions, in our pediatric surgery department, emergency surgery procedures were performed without delay.
Te primary purpose of this study was to compare two groups of patients with testicular torsion from two diferent time periods: before and during the COVID-19 pandemic. More specifcally, the cohort comprised boys with testicular torsion treated in the years 2019 and 2020 in our pediatric surgery department. We performed an analysis of their medical histories and focused on clinical symptoms and surgical treatment results to assess the potential impact of the pandemic on treatment outcomes in patients with testicular torsion.

Study Population.
Tis was a single-centre and retrospective cohort study. Te inclusion criteria were: pediatric patients aged under 18 years who had undergone emergent surgery due to acute testicular torsion. Te exclusion criterion was every other severe or chronic disease. A total of 44 boys aged 1 month-18 years who had undergone emergency scrotal exploration for acute testicular torsion between January 2019 and December 2020 were enrolled into the study. Te study protocol was approved by the local Ethics Committee of the Medical University of Bialystok, Poland (APK.002.392.2020).

Data Collection.
Te patients were divided in two groups. Te frst group (pre-COVID-19) comprised boys operated on in 2019 and the second one (COVID- 19) consisted of children operated on during the COVID-19 pandemic throughout 2020. We compared the two groups in terms of demographic data, local and general symptoms, and treatment outcomes. Laboratory tests and Doppler scrotal ultrasound were performed in all patients. We compared these results and intraoperative fndings (degree of torsion, determined by assessing the color of the testicle 5 minutes after detorsion, using an intraoperative scale (ITSC, Intraoperative Testis Color Scale)) [5], methods of surgical intervention, antibiotic therapy, length of operation and hospitalization, and followup. All patients in 2020 were operated after obtaining the result of COVID-19 Antigen Rapid Test. Standard surgical procedures used in our department involved scrotal exploration through a transversal incision, manual testicular detorsion, wrapping the testis with warm saline-soaked gauze, and intraoperative (5 minutes after detorsion) assessment of color of the affected testis on a visual scale (ITSC) [5]: 1-normal/pink, 2-mottled pink/light blue, 3-light blue, 4-dark blue/ purple, 5-black, and 6-hemorrhagic/necrotic. We divided the patients into two groups: the frst with scores 1-3 and the second with scores 4-6. Te next step was orchiectomy or orchiopexy, depending on the viability of the gonad. Testicular fxation was performed by suturing of the tunica albuginea to the dartos layer with 2 or 3 single absorbable 3-0 or 4-0 stitches along the vertical axis and in the lower pole of the testis. In addition, when a testicular appendage was found, it was removed.

Statistical Analysis.
Biostatistical processing of the obtained data was performed with the use of GraphPad Prism 9 (GraphPad Software Inc., San Diego, CA, USA). Medians with 25−75th percentiles (interquartile range) were used to summarize the quantitative variables, whereas absolute and relative (percentage) values were used to present qualitative data. For comparison of the diferences between studied groups, the nonparametric Mann-Whitney test was used. Te Chi-square test was applied for the evaluation of changes in the distribution of qualitative parameters. Relative risk analysis was performed with the use of Fisher's exact test with a 95% confdence interval, calculated using Koopman asymptomatic score. Diferences were considered statistically signifcant with p-value below 0.05 and indicated within graphs or tables with exact values or asterisks: * -p < 0.05, * * -p < 0.01, * * * -p < 0.001, and * * * * -p < 0.0001.

Results
Medical charts of 44 children diagnosed and operated on because of testicular torsion in the pediatric surgery and urology department between 2019 and 2020 were analyzed.
Te two groups did not difer signifcantly in terms of age, number of cases, or demographic data (Table 1).
In the year 2019, before the COVID-19 pandemic, 24 boys were operated on because of testicular torsion; their median age was 13.4 years, including three neonates (1month-old, 6-month-old, and 7-month-old). In the year 2020, during the pandemic, 20 boys were operated on, with a median age of 14.5 years, including one 4-month-old neonate. In both groups, patients lived mainly in urban areas: 58% patients in 2019 and 80% patients in 2020.
We analyzed the local and general symptoms of testicular torsion (Table 1). Te general symptoms, such as pain location, vomiting, or fever were not statistically diferent between the COVID-19 period and the pre-COVID-19 year. In both groups, the main manifestation was testicular pain without abdominal pain, fever, or vomiting. In both groups, scrotal edema and erythema predominated among the local symptoms (Table 2).
Te results of the laboratory tests did not refect the status of the gonad. Before the pandemic, the median white blood cell count was 10.33 × 10 9 /L, compared to 11.75 × 10 9 /L during the pandemic. Likewise, the median level of CRP in the frst group was 0.66 mg/ml, compared with 0.60 mg/ml in the second (Table 1).
We also analyzed Doppler ultrasound fndings (Table 3). Before the pandemic, in 65% cases testicles were heterogeneous vs. 78% during the pandemic. 45% of the twisted testicles in the frst group were described as hypoechoic, 45% as isoechoic, and 10% as hyperechoic vs. 29% as hypoechoic, 50% as isoechoic, and 21% as hyperechoic in the second group. We noticed that in 2019, ultrasound examination showed absence of blood fow in the afected testicle in 62% of cases vs. 80% in 2020. Te last parameter that we evaluated using USG was the testicle position. Tere were four possibilities: transversal, rotated, inguinal, and elevated position. We found no diference between both groups of patients as regards this parameter.
During the pandemic year of 2020, our department did not change the protocols of treatment for testicular torsion, apart from introducing COVID-19 Antigen Rapid Tests before surgery. Tere were no patients with positive results. Te time from admission to surgery was nearly identical: 75 minutes (52.25-98.50) in 2019 vs. 76 minutes (64.50-101.50) in 2020. Furthermore, the mean duration of scrotal revision was also similar: 25 minutes in 2019 vs. 20 minutes in 2020. Likewise, there was no diference in the mean length of hospitalization: 24 hours in both groups. Tere was a signifcant diference between the degrees of testicle twisting. In 2019, the mean degree was 360°, while in   2020−540°. Interestingly, a higher degree of testicular rotation did not infuence the rate of orchiectomy. Incidence of orchiectomy was also not signifcantly diferent between the two time periods: 21% (5/19) in the pre-COVID-19 period and 35% (7/13) during 2020. In both groups, the frequency of testicular appendage torsion was 42% (10/24 and 8/19 cases, respectively). In both groups, the majority of patients fell into the 1-3 categories on the ITSC scale (Table 4).
Tere was no statistically signifcant diference in regards to the antibiotic therapy in patients treated in 2019 vs. 2020. However, the variety of protocol treatment was wide ( Figure 1).
No perioperative complications were recorded in either of the groups. Tere were no readmissions during either of the followup periods. Tree cases of postoperative testicular atrophy were noted in the pre-COVID-19 group.
We also assessed the relative risk of orchiectomy in the context of selected parameters ( Figure 2).
And, it is found that boys without scrotal erythema had more than 7 times lower risk of orchiectomy than patients with this local symptom. Te diference was statistically signifcant. Lack of scrotal edema was associated with a fourfold lower risk of orchiectomy. Te risk of testicular loss was 16 times lower when the duration of symptoms was below 12 hours. Similarly, patients with lower scores on the ITCS scale had a 16 times lower risk of orchiectomy. WBC below 10 4 /μl and CRP below 10 mg/ml were also associated with lower risk of orchiectomy (3.5 and 4 times, respectively). In addition, lack of testicular heterogeneity in scrotal ultrasound was associated with a 6 times lower risk of orchiectomy. Similarly, we analyzed the risk of qualifcation into low [1][2][3] or high [4][5][6] ITCS score groups in relation to laboratory parameters and ultrasound fndings (Figure 3).
Patients with normal leukocytosis had a 4 times higher chance of a lower score on the ITCS scale. Moreover boys with lower CRP levels had a 2 times greater chance of a lower ITCS score. Patients without testicular heterogeneity in USG had a 4 times higher possibility of being in a low ITSC group. Patients with testicular torsion below 360°had a 2 times higher chance of having a lower ITCS score.

Discussion
Te COVID-19 pandemic posed a challenge not only in terms of providing medical treatment but also in the functioning of the entire healthcare system. Testicular torsion is one of the most time-sensitive paediatric emergencies: surgical intervention during the frst few hours from the onset of the symptoms increases the chance of testicular salvage. Similarly to other authors investigating this matter, during the frst wave of the outbreak, we did not observe a statistically signifcant diference in the time from the onset of the symptoms to the admission to the emergency department [6][7][8]. On the other hand, Pogorelic et al. noted a lengthening of that period to up to 14 hours during the COVID-19 pandemic, which may be the cause of higher rates of orchiectomy in that time in Croatia [9]. Holzman's study [10] also found that the median time from symptom onset to emergency department presentation during COVID-19 was 17.9 hours, and hence, in the COVID-19 group, 42% of patients underwent orchiectomy compared to 29% of the patients with pre-COVID time. Although we did not observe a statistically signifcant rise in the orchiectomy rate, the median time from the onset of symptoms to admission to hospital has risen from 6.5 hours (2019) to 8.5 hours (2020). Taking into consideration that testicular torsion is one of the most time-sensitive emergencies, 2 hours might result in irreversible changes in the testis which sometimes leads to testicular atrophy and eventually orchiectomy. In the latest population-based study [11] comprising 5,694 patients with testicular torsion, the rate of orchiectomy was 24.78%, with the highest rate in children   Emergency Medicine International from 0 to 1 year (45.37%) and males older than 50 years (74.38%). Tis is similar to another study [12] on 1,713 pediatric patients with testicular torsion and a 28% rate of orchiectomy. Both results are comparable with our fndings: we observed a 25% rate of testicular resection in our patients with testicular torsion. According to Zvizdic et al., the duration of symptoms is the only predictor of testicular salvage [13]. Since the time from the onset of symptoms to access to an emergency department remains under parental control, in our opinion the focus should be placed on providing proper treatment as soon as possible after admission to the hospital, particularly shortening the time to surgery. Our fndings reveal no signifcant diferences between the time from admission to surgical treatment or the mean duration of scrotal revision. Terefore, we can conclude that the quality of medical care provided for children in our department during the COVID-19 pandemic was comparable to that during the studied pre-COVID-19 period. According to Gold et al. [14], quality of healthcare is an independent factor determining testicular survival. It seems signifcant that in our hospital the time from admission to surgery was nearly identical before and during the pandemic period. Moreover, this time was signifcantly shorter when compared to other analyzes. In a recent study by El-Mezayen et al. the time from admission to surgery was 127-196 minutes [15], while in another by Gold et al. 135 minutes [14]. Although the COVID-19 pandemic has signifcantly limited access to the healthcare system, and some studies showed delays in admission to EDs and a more severe course of disease, it does not seem to have afected patients with testicular torsion [16,17]. Tis may be due to the signifcantly smaller number of COVIDpositive pediatric patients compared to adults [18]. On the other hand, neither patients, nor caregivers, underestimated disturbing symptoms such as acute testicular pain.
According to our survey, the typical patient with testicular torsion is a teenager with acute pain of the left testicle, without other local or general symptoms. Despite the high sensitivity and specifcity of Doppler scrotal ultrasound, this investigation does not always provide an accurate diagnosis    Emergency Medicine International [19]. Nevertheless, as recommended by our protocol, we performed ultrasound in all patients. Typical fndings were heterogeneity of the gonads and abnormal testicle position.
Absence of blood fow in the gonads in ultrasound examination was found in 71% cases and did not correlate with the rate of orchiectomy (25%). It needs to be highlighted that surgical exploration must be performed every time when history and symptoms indicate acute testicular torsion, regardless of the result of Doppler scrotal ultrasound. Biochemical blood results did not correlate with the local symptoms. However, normal WBC and CRP levels were more commonly observed in patients with lower ITCS scores. It should be added that there are no clear guidelines on antibiotic prophylaxis. In our center, all patients with testicular torsion received antibiotic treatment, regardless of laboratory results or intraoperative fndings.

Conclusion
New organization of the Polish health care system during the COVID-19 pandemic did not delay proper diagnosis or treatment of testicular torsion in the pediatric population. In conclusion, fear of infection and limited availability of GP care did not afect the rate of surgical orchiectomy after testicular torsion in boys.

Data Availability
Te data used to support the fndings of this study are included within the article.

Conflicts of Interest
Te authors declare that there are no conficts of interest.

Authors' Contributions
Marta Komarowska conceptualized the study, proposed the methodology, and investigated the study, wrote the the original draft, and wrote the the review and edited; Małgorzata Kowalska managed the software, gathered the resources, and curated the data; Kamil Grubczak formally analysed the study and visualized the study; Alicja Pawelczyk managed the software, gathered the resources, and curated the data; Adam Hermanowicz validated the study; Wojciech Debek carried out the project administration; Ewa Matuszczak supervised the study and carried out the funding acquisition. All authors reviewed the manuscript and approved the fnal version of the manuscript.